DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp.

Summary: This study examines a natural consortium of halophilic archaea, comprising xylan-degrading Halorhabdus sp. SVX81, consortium cohabitant Haloferax volcanii SVX82 (formerly H. lucentense SVX82), and its DPANN ectosymbiont Ca. Nanohalococcus occultus SVXNc. Transcriptomics and targeted metabol...

Full description

Saved in:
Bibliographic Details
Main Authors: Oleg N. Reva, Violetta La Cono, Laura Marturano, Francesca Crisafi, Francesco Smedile, Manasi Mudaliyar, Debnath Ghosal, Elena A. Selivanova, Marina E. Ignatenko, Manuel Ferrer, Laura Fernandez-Lopez, Mart Krupovic, Michail M. Yakimov
Format: Article
Language:English
Published: Elsevier 2025-02-01
Series:iScience
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S2589004225000082
Tags: Add Tag
No Tags, Be the first to tag this record!
_version_ 1832586252045516800
author Oleg N. Reva
Violetta La Cono
Laura Marturano
Francesca Crisafi
Francesco Smedile
Manasi Mudaliyar
Debnath Ghosal
Elena A. Selivanova
Marina E. Ignatenko
Manuel Ferrer
Laura Fernandez-Lopez
Mart Krupovic
Michail M. Yakimov
author_facet Oleg N. Reva
Violetta La Cono
Laura Marturano
Francesca Crisafi
Francesco Smedile
Manasi Mudaliyar
Debnath Ghosal
Elena A. Selivanova
Marina E. Ignatenko
Manuel Ferrer
Laura Fernandez-Lopez
Mart Krupovic
Michail M. Yakimov
author_sort Oleg N. Reva
collection DOAJ
description Summary: This study examines a natural consortium of halophilic archaea, comprising xylan-degrading Halorhabdus sp. SVX81, consortium cohabitant Haloferax volcanii SVX82 (formerly H. lucentense SVX82), and its DPANN ectosymbiont Ca. Nanohalococcus occultus SVXNc. Transcriptomics and targeted metabolomics demonstrated that the tripartite consortium outperformed individual and the Halorhabdus sp. SVX81 with H. volcanii SVX82 bipartite cultures in xylan degradation, exhibiting a division of labor: the DPANN symbiont processed glycolysis products, while other members performed xylan depolymerization and biosynthesis of essential compounds. Electron microscopy and cryo-electron tomography revealed the formation of heterocellular biofilms interlinked by DPANN cells. The findings demonstrated that DPANN symbionts can interact directly with other members of microbial communities, which are not their primary hosts, influencing their gene expression. However, DPANN proliferation requires their primary host presence. The study highlights the collective contribution of consortium members to xylan degradation and their potential for biotechnological applications in the management of hypersaline environments.
format Article
id doaj-art-2b9fc5ea5dde47288e758b266c2bd7f0
institution Kabale University
issn 2589-0042
language English
publishDate 2025-02-01
publisher Elsevier
record_format Article
series iScience
spelling doaj-art-2b9fc5ea5dde47288e758b266c2bd7f02025-01-26T05:04:34ZengElsevieriScience2589-00422025-02-01282111749DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp.Oleg N. Reva0Violetta La Cono1Laura Marturano2Francesca Crisafi3Francesco Smedile4Manasi Mudaliyar5Debnath Ghosal6Elena A. Selivanova7Marina E. Ignatenko8Manuel Ferrer9Laura Fernandez-Lopez10Mart Krupovic11Michail M. Yakimov12Department of Biochemistry, Genetics and Microbiology, Centre for Bioinformatics and Computational Biology, University of Pretoria, 0002 Pretoria, South Africa; Corresponding authorExtreme Microbiology, Biotechnology and Astrobiology Group, Institute of Polar Sciences, ISP-CNR, 98122 Messina, ItalyExtreme Microbiology, Biotechnology and Astrobiology Group, Institute of Polar Sciences, ISP-CNR, 98122 Messina, ItalyExtreme Microbiology, Biotechnology and Astrobiology Group, Institute of Polar Sciences, ISP-CNR, 98122 Messina, ItalyExtreme Microbiology, Biotechnology and Astrobiology Group, Institute of Polar Sciences, ISP-CNR, 98122 Messina, ItalyDepartment of Biochemistry and Pharmacology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Melbourne, 3052 VIC, Australia; ARC Centre for Cryo-electron Microscopy of Membrane Proteins, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, 3052 VIC, AustraliaDepartment of Biochemistry and Pharmacology, Bio21 Molecular Science and Biotechnology Institute, The University of Melbourne, Melbourne, 3052 VIC, Australia; ARC Centre for Cryo-electron Microscopy of Membrane Proteins, Bio21 Molecular Science and Biotechnology Institute, University of Melbourne, Parkville, 3052 VIC, AustraliaOrenburg Federal Research Center, Institute for Cellular and Intracellular Symbiosis, Ural Branch of Russian Academy of Sciences, 460000 Orenburg, RussiaOrenburg Federal Research Center, Institute for Cellular and Intracellular Symbiosis, Ural Branch of Russian Academy of Sciences, 460000 Orenburg, RussiaInstituto de Catalisis y Petroleoquimica (ICP), CSIC, 28049 Madrid, SpainInstituto de Catalisis y Petroleoquimica (ICP), CSIC, 28049 Madrid, SpainInstitut Pasteur, Université Paris Cité, CNRS UMR6047, Archaeal Virology Unit, 75015 Paris, FranceExtreme Microbiology, Biotechnology and Astrobiology Group, Institute of Polar Sciences, ISP-CNR, 98122 Messina, Italy; Corresponding authorSummary: This study examines a natural consortium of halophilic archaea, comprising xylan-degrading Halorhabdus sp. SVX81, consortium cohabitant Haloferax volcanii SVX82 (formerly H. lucentense SVX82), and its DPANN ectosymbiont Ca. Nanohalococcus occultus SVXNc. Transcriptomics and targeted metabolomics demonstrated that the tripartite consortium outperformed individual and the Halorhabdus sp. SVX81 with H. volcanii SVX82 bipartite cultures in xylan degradation, exhibiting a division of labor: the DPANN symbiont processed glycolysis products, while other members performed xylan depolymerization and biosynthesis of essential compounds. Electron microscopy and cryo-electron tomography revealed the formation of heterocellular biofilms interlinked by DPANN cells. The findings demonstrated that DPANN symbionts can interact directly with other members of microbial communities, which are not their primary hosts, influencing their gene expression. However, DPANN proliferation requires their primary host presence. The study highlights the collective contribution of consortium members to xylan degradation and their potential for biotechnological applications in the management of hypersaline environments.http://www.sciencedirect.com/science/article/pii/S2589004225000082BiochemistryMicrobiologyEnvironmental Biotechnology
spellingShingle Oleg N. Reva
Violetta La Cono
Laura Marturano
Francesca Crisafi
Francesco Smedile
Manasi Mudaliyar
Debnath Ghosal
Elena A. Selivanova
Marina E. Ignatenko
Manuel Ferrer
Laura Fernandez-Lopez
Mart Krupovic
Michail M. Yakimov
DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp.
iScience
Biochemistry
Microbiology
Environmental Biotechnology
title DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp.
title_full DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp.
title_fullStr DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp.
title_full_unstemmed DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp.
title_short DPANN symbiont of Haloferax volcanii accelerates xylan degradation by the non-host haloarchaeon Halorhabdus sp.
title_sort dpann symbiont of haloferax volcanii accelerates xylan degradation by the non host haloarchaeon halorhabdus sp
topic Biochemistry
Microbiology
Environmental Biotechnology
url http://www.sciencedirect.com/science/article/pii/S2589004225000082
work_keys_str_mv AT olegnreva dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT violettalacono dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT lauramarturano dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT francescacrisafi dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT francescosmedile dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT manasimudaliyar dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT debnathghosal dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT elenaaselivanova dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT marinaeignatenko dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT manuelferrer dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT laurafernandezlopez dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT martkrupovic dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp
AT michailmyakimov dpannsymbiontofhaloferaxvolcaniiacceleratesxylandegradationbythenonhosthaloarchaeonhalorhabdussp